Heme-Oxygenase i and PCG-1α Regulate Mitochondrial Biogenesis via Microglial Activation of Alpha7 Nicotinic Acetylcholine Receptors Using PNU282987

Antioxidants and Redox Signaling

Volumn 27, Issue 2, 2017, Pages 93-105

  Navarro, Elisa ^a,b   Gonzalez Lafuente, Laura ^a   Pérez Liébana, Irene ^a   Buendia, Izaskun ^a,b   López Bernardo, Elia ^b,c   Sánchez Ramos, Cristina ^d   Prieto, Ignacio ^d   Cuadrado, Antonio ^d   Satrustegui, Jorgina ^c   Cadenas, Susana ^b,c   Monsalve, Maria ^d   López, Manuela G ^a,b  

^a INSTITUTO TEÓFILO HERNANDO   (Spain)

^b Instituto de Investigación Sanitaria del Hospital Universitario de La Princesa   (Spain)

^c UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^d INSTITUTO DE INVESTIGACIONES BIOMÉDICAS ALBERTO SOLS   (Spain)

Author keywords

alpha 7 nicotinic receptors; heme oxygenase 1; microglia; mitochondrial biogenesis; PGC 1alpha; PNU282987

Indexed keywords

4 CHLORO N (3 QUINUCLIDINYL)BENZAMIDE; BUNGAROTOXIN RECEPTOR; HEME OXYGENASE 1; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; RESVERATROL; TRANSCRIPTION FACTOR NRF2; BENZAMIDE DERIVATIVE; BRIDGED BICYCLO COMPOUNDS; PNU-282987;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BODY WEIGHT; CELL ACTIVATION; CONTROLLED STUDY; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; GENE SILENCING; INTRACELLULAR SIGNALING; MICROGLIA; MITOCHONDRIAL BIOGENESIS; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL RESPIRATION; MOUSE; NONHUMAN; OXIDATIVE STRESS; OXYGEN CONSUMPTION; PRIORITY JOURNAL; PROMOTER REGION; ANIMAL; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; GENETICS; GLIA; INTRAPERITONEAL DRUG ADMINISTRATION; METABOLISM; MITOCHONDRION; ORGANELLE BIOGENESIS; PATHOLOGY; RAT;

ALPHA7 NICOTINIC ACETYLCHOLINE RECEPTOR; ANIMALS; BENZAMIDES; BRIDGED BICYCLO COMPOUNDS; CELLS, CULTURED; HEME OXYGENASE-1; INJECTIONS, INTRAPERITONEAL; MICE; MITOCHONDRIA; NEUROGLIA; NF-E2-RELATED FACTOR 2; ORGANELLE BIOGENESIS; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTOR GAMMA COACTIVATOR 1-ALPHA; RATS;

EID: 85021411402     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2016.6698     Document Type: Article

References (48)

1. Aquilano K, Baldelli S, Pagliei B, Cannata SM, Rotilio G, and Ciriolo MR. p53 Orchestrates the PGC-1alphamediated antioxidant response upon mild redox and metabolic imbalance. Antioxid Redox Signal 18: 386-399, 2013.
2. Bach FH. Heme oxygenase-1: A therapeutic amplification funnel. FASEB J 19: 1216-1219, 2005.
3. Baldelli S, Aquilano K, and Ciriolo MR. Punctum on two different transcription factors regulated by PGC-1alpha: Nuclear factor erythroid-derived 2-like 2 and nuclear respiratory factor 2. Biochim Biophys Acta 1830: 4137-4146, 2013.
4. Borniquel S, Garcia-Quintans N, Valle I, Olmos Y, Wild B, Martinez-Granero F, Soria E, Lamas S, and Monsalve M. Inactivation of Foxo3a and subsequent downregulation of PGC-1 alpha mediate nitric oxide-induced endothelial cell migration. Mol Cell Biol 30: 4035-4044, 2010.
5. Chaturvedi RK and Flint Beal M. Mitochondrial diseases of the brain. Free Radic Biol Med 63: 1-29, 2013.
6. Clausen BE, Burkhardt C, Reith W, Renkawitz R, and Forster I. Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res 8: 265-277, 1999.
7. Corona JC and Duchen MR. Impaired mitochondrial homeostasis and neurodegeneration: Towards new therapeutic targets? J Bioenerg Biomembr 47: 89-99, 2015.
8. De la Fuente M and Miquel J. An update of the oxidationinflammation theory of aging: The involvement of the immune system in oxi-inflamm-aging. Curr Pharm Des 15: 3003-3026, 2009.
9. Del Barrio L, Martin-de-Saavedra MD, Romero A, Parada E, Egea J, Avila J, McIntosh JM, Wonnacott S, and Lopez MG. Neurotoxicity induced by okadaic acid in the human neuroblastoma SH-SY5Y line can be differentially prevented by alpha7 and beta2∗ nicotinic stimulation. Toxicol Sci 123: 193-205, 2011.
10. Dominy JE and Puigserver P. Mitochondrial biogenesis through activation of nuclear signaling proteins. Cold Spring Harb Perspect Biol 5: 1-16, 2013.
11. Egea J, Buendia I, Parada E, Navarro E, Leon R, and Lopez MG. Anti-inflammatory role of microglial alpha7 nAChRs and its role in neuroprotection. Biochem Pharmacol 97: 463-472, 2015.
12. Egea J, Buendia I, Parada E, Navarro E, Leon R, and Lopez MG. Anti-inflammatory role of microglial alpha7 nAChRs and its role in neuroprotection. Biochem Pharmacol 97: 463-472, 2015.
13. Friedman JR and Nunnari J. Mitochondrial form and function. Nature 505: 335-343, 2014.
14. Janetzky B, Hauck S, Youdim MB, Riederer P, Jellinger K, Pantucek F, Zochling R, Boissl KW, and Reichmann H. Unaltered aconitase activity, but decreased complex I activity in substantia nigra pars compacta of patients with Parkinson's disease. Neurosci Lett 169: 126-128, 1994.
15. Kim SK, Joe Y, Zheng M, Kim HJ, Yu JK, Cho GJ, Chang KC, Kim HK, Han J, Ryter SW, and Chung HT. Resveratrol induces hepatic mitochondrial biogenesis through the sequential activation of nitric oxide and carbon monoxide production. Antioxid Redox Signal 20: 2589-2605, 2014.
16. Liang WS, Reiman EM, Valla J, Dunckley T, Beach TG, Grover A, Niedzielko TL, Schneider LE, Mastroeni D, Caselli R, Kukull W, Morris JC, Hulette CM, Schmechel D, Rogers J, and Stephan DA. Alzheimer's disease is associated with reduced expression of energy metabolism genes in posterior cingulate neurons. Proc Natl Acad Sci U S A 105: 4441-4446, 2008.
17. Lin J, Wu PH, Tarr PT, Lindenberg KS, St-Pierre J, Zhang CY, Mootha VK, Jager S, Vianna CR, Reznick RM, Cui L, Manieri M, Donovan MX, Wu Z, Cooper MP, Fan MC, Rohas LM, Zavacki AM, Cinti S, Shulman GI, Lowell BB, Krainc D, and Spiegelman BM. Defects in adaptive energy metabolism with CNS-linked hyperactivity in PGC-1alpha null mice. Cell 119: 121-135, 2004.
18. Mamiya T, Katsuoka F, Hirayama A, Nakajima O, Kobayashi A, Maher JM, Matsui H, Hyodo I, Yamamoto M, and Hosoya T. Hepatocyte-specific deletion of heme oxygenase-1 disrupts redox homeostasis in basal and oxidative environments. Tohoku J Exp Med 216: 331-339, 2008.
19. Martelli D, McKinley MJ, and McAllen RM. The cholinergic anti-inflammatory pathway: A critical review. Auton Neurosci 182: 65-69, 2014.
20. McMahon M, Itoh K, Yamamoto M, and Hayes JD. Keap1-dependent proteasomal degradation of transcription factor Nrf2 contributes to the negative regulation of antioxidant response element-driven gene expression. J Biol Chem 278: 21592-21600, 2003.
21. Mosconi L, Tsui WH, De Santi S, Li J, Rusinek H, Convit A, Li Y, Boppana M, and de Leon MJ. Reduced hippocampal metabolism in MCI and AD: Automated FDG-PET image analysis. Neurology 64: 1860-1867, 2005.
22. Navarro E, Buendia I, Parada E, Leon R, Jansen-Duerr P, Pircher H, Egea J, and Lopez MG. Alpha7 nicotinic receptor activation protects against oxidative stress via hemeoxygenase I induction. Biochem Pharmacol 97: 473-481, 2015.
23. Norden DM, Fenn AM, Dugan A, and Godbout JP. TGFbeta produced by IL-10 redirected astrocytes attenuates microglial activation. Glia 62: 881-895, 2014.
24. Norden DM, Trojanowski PJ, Villanueva E, Navarro E, and Godbout JP. Sequential activation of microglia and astrocyte cytokine expression precedes increased iba-1 or GFAP immunoreactivity following systemic immune challenge. Glia 64: 300-316, 2015.
25. Nunnari J and Suomalainen A. Mitochondria: In sickness and in health. Cell 148: 1145-1159, 2012.
26. Olmos Y, Sanchez-Gomez FJ, Wild B, Garcia-Quintans N, Cabezudo S, Lamas S, and Monsalve M. SirT1 regulation of antioxidant genes is dependent on the formation of a FoxO3a/PGC-1alpha complex. Antioxid Redox Signal 19: 1507-1521, 2013.
27. Otterbein LE, Soares MP, Yamashita K, and Bach FH. Heme oxygenase-1: Unleashing the protective properties of heme. Trends Immunol 24: 449-455, 2003.
28. Parada E, Buendia I, Navarro E, Avendano C, Egea J, and Lopez MG. Microglial HO-1 induction by curcumin provides antioxidant, antineuroinflammatory, and glioprotective effects. Mol Nutr Food Res 59: 1690-1700, 2015.
29. Parada E, Egea J, Buendia I, Negredo P, Cunha AC, Cardoso S, Soares MP, and Lopez MG. The microglial alpha7-acetylcholine nicotinic receptor is a key element in promoting neuroprotection by inducing heme oxygenase-1 via nuclear factor erythroid-2-related factor 2. Antioxid Redox Signal 19: 1135-1148, 2013.
30. Parada E, Egea J, Romero A, del Barrio L, Garcia AG, and Lopez MG. Poststress treatment with PNU282987 can rescue SH-SY5Y cells undergoing apoptosis via alpha7 nicotinic receptors linked to a Jak2/Akt/HO-1 signaling pathway. Free Radic Biol Med 49: 1815-1821, 2010.
31. Parker WD, Jr., Parks JK, and Swerdlow RH. Complex I deficiency in Parkinson's disease frontal cortex. Brain Res 1189: 215-218, 2008.
32. Piantadosi CA, Carraway MS, Babiker A, and Suliman HB. Heme oxygenase-1 regulates cardiac mitochondrial biogenesis via Nrf2-mediated transcriptional control of nuclear respiratory factor-1. Circ Res 103: 1232-1240, 2008.
33. Piantadosi CA, Withers CM, Bartz RR, MacGarvey NC, Fu P, Sweeney TE, Welty-Wolf KE, and Suliman HB. Heme oxygenase-1 couples activation of mitochondrial biogenesis to anti-inflammatory cytokine expression. J Biol Chem 286: 16374-16385, 2011.
34. Picciotto MR and Zoli M. Nicotinic receptors in aging and dementia. J Neurobiol 53: 641-655, 2002.
35. Quik M, Zhang D, McGregor M, and Bordia T. Alpha7 nicotinic receptors as therapeutic targets for Parkinson's disease. Biochem Pharmacol 97: 399-407, 2015.
36. Rapoport SI. In vivo PET imaging and postmortem studies suggest potentially reversible and irreversible stages of brain metabolic failure in Alzheimer's disease. Eur Arch Psychiatry Clin Neurosci 249 Suppl 3: 46-55, 1999.
37. Rayamajhi N, Kim SK, Go H, Joe Y, Callaway Z, Kang JG, Ryter SW, and Chung HT. Quercetin induces mitochondrial biogenesis through activation of HO-1 in HepG2 cells. Oxid Med Cell Longev 2013: 154279, 2013.
38. Rhein V, Song X, Wiesner A, Ittner LM, Baysang G, Meier F, Ozmen L, Bluethmann H, Drose S, Brandt U, Savaskan E, Czech C, Gotz J, and Eckert A. Amyloid-beta and tau synergistically impair the oxidative phosphorylation system in triple transgenic Alzheimer's disease mice. Proc Natl Acad Sci U S A 106: 20057-20062, 2009.
39. Scarpulla RC. Transcriptional paradigms in mammalian mitochondrial biogenesis and function. Physiol Rev 88: 611-638, 2008.
40. Scarpulla RC, Vega RB, and Kelly DP. Transcriptional integration of mitochondrial biogenesis. Trends Endocrinol Metab 23: 459-466, 2012.
41. Schapira AH, Cooper JM, Dexter D, Clark JB, Jenner P, and Marsden CD. Mitochondrial complex I deficiency in Parkinson's disease. J Neurochem 54: 823-827, 1990.
42. St-Pierre J, Drori S, Uldry M, Silvaggi JM, Rhee J, Jager S, Handschin C, Zheng K, Lin J, Yang W, Simon DK, Bachoo R, and Spiegelman BM. Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators. Cell 127: 397-408, 2006.
43. Stevens DA, Lee Y, Kang HC, Lee BD, Lee YI, Bower A, Jiang H, Kang SU, Andrabi SA, Dawson VL, Shin JH, and Dawson TM. Parkin loss leads to PARIS-dependent declines in mitochondrial mass and respiration. Proc Natl Acad Sci U S A 112: 11696-11701, 2015.
44. Streit WJ. Microglial senescence: does the brain's immune system have an expiration date? Trends Neurosci 29: 506-510, 2006.
45. Streit WJ and Xue QS. Life and death of microglia. J Neuroimmune Pharmacol 4: 371-379, 2009.
46. Suliman HB, Carraway MS, Tatro LG, and Piantadosi CA. A new activating role for CO in cardiac mitochondrial biogenesis. J Cell Sci 120: 299-308, 2007.
47. Suliman HB, Sweeney TE, Withers CM, and Piantadosi CA. Co-regulation of nuclear respiratory factor-1 by NFkappaB and CREB links LPS-induced inflammation to mitochondrial biogenesis. J Cell Sci 123: 2565-2575, 2010.
48. Wang H, Yu M, Ochani M, Amella CA, Tanovic M, Susarla S, Li JH, Yang H, Ulloa L, Al-Abed Y, Czura CJ, and Tracey KJ. Nicotinic acetylcholine receptor alpha7 subunit is an essential regulator of inflammation. Nature 421: 384-388, 2003.